Comparative gene regulatory network mapping of Brassicaceae members with differential drought tolerance

Authors:
  • RPRamakrishnan Pandiarajan
    Ramakrishnan Pandiarajan
  • CLChung-Wen Lin
    Chung-Wen Lin
  • MSMayra Sauer
    Mayra Sauer
  • SRSimin T Rothballer
    Simin T Rothballer
  • NRNora Marin-De la Rosa
    Nora Marin-De la Rosa
  • PSPatrick Schwehn
    Patrick Schwehn
  • EPEleftheria Papadopoulou
    Eleftheria Papadopoulou
  • BMBenedikt Mairhörmann
    Benedikt Mairhörmann
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Abstract
Climate change is projected to intensify weather extremes like droughts that threaten global crop yields. While many crops are sensitive to water deprivation, they have drought-tolerant wild relatives; however, the molecular basis for this differential tolerance among closely related species remains unclear. We previously investigated this using transcriptomics in the Brassicaceae family, comparing the drought-sensitive reference plant Arabidopsis thaliana (Ath) with its drought-tolerant relatives Arabidopsis lyrata (Aly) and Eutrema salsugineum (Esa) , uncovering key differences that may underlie their respective phenotypes. Here, to elucidate the regulatory architecture driving these differences, we mapped drought-responsive gene regulatory networks (GRNs) for all three species using the yeast one-hybrid (Y1H) approach. We cloned promoters of orthologs with divergent drought-induced expression patterns and screened them against the Ath transcription factor (TF) collection, generating a quality-controlled cross-species drought-responsive GRN map encompassing 1,137 high-confidence TF-promoter interactions. Comparative analysis revealed that the tolerant species share greater regulatory similarity and exhibit higher network connectivity than Ath . An Esa -specific expansion of bZIP TF interactions was observed, consistent with an enrichment of G-box motifs in its genome and in drought-upregulated genes. Several observed changes affect the ABA signalling pathway: Ath gained a susceptibility linked GBF3- CYP707A1 edge, whereas Esa acquired tolerance associated ABF- mTERF10 interactions. Furthermore, network-rewiring analysis uncovered a novel role for ASIL2 in stress response. Finally, our network highlights TFs (CSDP1, ERF4, HB6, and MYB73) that likely contribute to the “stress-primed” state of Aly and Esa . Our work provides a broadly applicable framework for comparative GRN mapping and a valuable resource for improving drought tolerance in crops.
Funding Information
  • European Union’s Horizon 2020 Research and Innovation Programme (648420)

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