Reversible protein phosphorylation is a post-translational modification involved in virtually all plant processes, as it mediates protein activity and signal transduction. Here, we probe dynamic protein phosphorylation during de novo shoot organogenesis in Arabidopsis thaliana. We find that application of three kinase inhibitors in various time intervals has different effects on root explants. Short exposures to the putative histidine (His) kinase inhibitor TCSA during the initial days on shoot induction medium (SIM) are detrimental for regeneration in seven natural accessions. Investigation of cytokinin signaling mutants, as well as reporter lines for hormone responses and shoot markers, suggests that TCSA impedes cytokinin signal transduction via AHK3, AHK4, AHP3, and AHP5. A mass spectrometry-based phosphoproteome analysis further reveals profound deregulation of Ser/Thr/Tyr phosphoproteins regulating protein modification, transcription, vesicle trafficking, organ morphogenesis, and cation transport. Among TCSA-responsive factors are prior candidates with a role in shoot apical meristem patterning, such as AGO1, BAM1, PLL5, FIP37, TOP1ALPHA, and RBR1, as well as proteins involved in polar auxin transport (e.g., PIN1) and brassinosteroid signaling (e.g., BIN2). Putative novel regeneration determinants regulated by TCSA include RD2, AT1G52780, PVA11, and AVT1C, while NAIP2, OPS, ARR1, QKY, and aquaporins exhibit differential phospholevels on control SIM. LC-MS/MS data are available via ProteomeXchange with identifier PXD030754.

Biotechnology Research and Development Institute Can Tho University Can Tho Vietnam

Center for Plant Systems Biology VIB Ghent Belgium

Department of Plant Biotechnology and Bioinformatics Faculty of Sciences Ghent University Ghent Belgium

HortiCell Department of Plants and Crops Faculty of Bioscience Engineering Ghent University Ghent Belgium

Lab of Plant Growth Analysis Ghent University Global Campus Incheon South Korea

Laboratory of Functional Genomics and Proteomics Faculty of Science National Centre for Biomolecular Research Masaryk University Brno Czechia

Mendel Centre for Plant Genomics and Proteomics Central European Institute of Technology Masaryk University Brno Czechia

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Cytokinins - regulators of de novo shoot organogenesis