LIFERING, an E3 ligase ubiquitinates the acyl-CoA dehydrogenase-like protein IBR3, and coordinates cell proliferation and death upon DNA damage

Plants rapidly respond to environmental changes to ensure an optimal balance between growth and survival with intact genome. Here, we show that a DNA damage response gene, which we named LIFERING, is under the direct and independent regulation of ATM/ATR-SOG1 and RBR pathways. We demonstrate that LIFERING upon DNA damage plays an essential role in maintaining the balance between cell proliferation and cell death. Downstream of RBR, it is required to maintain proliferation, and in response to DNA damaging agents it initiates a cell death accompanied by rapid elongation and differentiation of the transit amplifying cells in the root meristem. LIFERING is a RING-between-RING E3 ligase; its ligase activity is dependent on the Cys392 residue located in the BRcat domain, responsible for the coordination of zinc ion binding. Using proximity labelling, we identified the acyl-CoA dehydrogenase-like protein IBR3, which is involved in the conversion of indole-3-butyric acid (IBA) to indole-3-acetic acid (IAA), as one of its targets. We provide evidence that IBR3 is ubiquitinated at several Lys residues in the presence of LIFERING. Our findings show that LIFERING rapidly responds to DNA damage and via ubiquitination of IBR3, is likely to be involved in the regulation of free-auxin level, indicating a link between DNA damage response and auxin regulation in the root.