Gene regulation is a dynamic process in which transcription factors (TFs) play an important role in controlling spatiotemporal gene expression. To enhance our global understanding of regulatory interactions in Arabidopsis thaliana, different regulatory input networks capturing complementary information about DNA motifs, open chromatin, TF-binding and expression-based regulatory interactions were combined using a supervised learning approach, resulting in an integrated gene regulatory network (iGRN) covering 1,491 TFs and 31,393 target genes (1.7 million interactions). This iGRN outperforms the different input networks to predict known regulatory interactions and has a similar performance to recover functional interactions compared to state-of-the-art experimental methods. The iGRN correctly inferred known functions for 681 TFs and predicted new gene functions for hundreds of unknown TFs. For regulators predicted to be involved in reactive oxygen species (ROS) stress regulation, we confirmed in total 75% of TFs with a function in ROS and/or physiological stress responses. This includes 13 ROS regulators, previously not connected to any ROS or stress function, that were experimentally validated in our ROS-specific phenotypic assays of loss- or gain-of-function lines. In conclusion, the presented iGRN offers a high-quality starting point to enhance our understanding of gene regulation in plants by integrating different experimental data types.
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We thank C. Bolle (SCL13), X. Chen (ARF3), Y.-F. Chen (WRKY45), D. Fernandez (AGL15), H. Frerigmann (MYB51, MYB122), M. Gaj (ERF022), T. Gigolashvili (MYB51), D. Hegedus (SCL15), L. Hennig (AGL19), I. Hwang (BME3), Z. Liu (TSO1), L. Østergaard (ARF3), J. Paz-Ares (PHL1) and O. Van Aken (WRKY45) for kindly providing the Arabidopsis mutant lines noted in parentheses. We thank Z. Joly-Lopez and O. Wilkins for providing in-depth comments on an earlier version of the manuscript, as well as C. Ferrari and I. Dissanayake for proofreading. I.D.C. is supported by the Research Foundation Flanders (postdoctoral fellowship 12N2415N and grant for a long stay abroad V400620N). J.V.d.V. is indebted to the Agency for Innovation by Science and Technology in Flanders for a predoctoral fellowship. X.L. and L.L. are supported by the China Scholarship Council for a PhD fellowship (201706910099 and 201808530499). F.V.B. is supported by the Fonds Wetenschappelijk Onderzoek—Vlaanderen (FWO) and the Fonds de la Recherche Scientifique (FNRS) under EOS project no. 30829584 and the Research Foundation Flanders (project nos. G0D7914N and G055416N).
The authors declare no competing interests.
Peer review information Nature Plants thanks Oscar Lorenzo and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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De Clercq, I., Van de Velde, J., Luo, X. et al. Integrative inference of transcriptional networks in Arabidopsis yields novel ROS signalling regulators. Nat. Plants 7, 500–513 (2021). https://doi.org/10.1038/s41477-021-00894-1
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