Multi-omics profiling reveals common and specific molecular responses to butenolide perception

Abstract Strigolactones (SLs) and Karrikins (KARs) are butenolide compounds that have been characterized to act like phytohormones. While SLs are synthesized endogenously in plants from carotenoids, KARs are a known constituent of wildfire smoke emanating from the combustion of carbohydrates in burning plant tissues. Despite their different sources of origin, they have similar chemical structures and are perceived through similar receptor complexes. However, the compound-specific molecular pathways downstream of these two signalling molecules remains to be elucidated. Hereby, we adopt an integrated approach combining transcriptome, proteome, proteogenome and metabolome profiling to compare the molecular responses of seeds and seedlings to the synthetic strigolactone analog, rac-GR24 and to the karrikinolide, KAR1 in Arabidopsis seeds or seedlings. This multi-omics approach allowed us to delineate the key conserved, and compound-specific, regulators such as transcription factors, splicing-related proteins, and primary metabolites that could play important functional roles in establishing the signaling response to these butenolides. Correlational analysis suggested differential splicing and metabolite regulation in response to rac-GR24 and KARs suggesting potential molecular targets including the TCA cycle. Treatment of mutants of key enzymes of energy metabolism, identified in the above studies, revealed that these mutants showed altered metabolic responses to butenolide treatment. In summary, our integrative dataset reveals strong associations between butenolide treatment and TCA cycle related changes across multiple molecular levels, and provides a foundation for generating testable hypotheses on how these signals interface with energy metabolism.