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Plants generate organs continuously during post-embryonic development, thus how to preserve stem cells in changing environments is crucial for their survival. Genotoxic stress threatens genome stability in all somatic cells, whereas, in the meristem, only stem cells undergo cell death in response to DNA damage, followed by stem cell replenishment. It was previously shown that inhibition of downward auxin flow in roots participates in DNA damage-induced stem cell death; however, how cell death is confined to stem cells in tissues with reduced auxin content remains elusive. Here we show that, in response to DNA double-strand breaks, the Aux/IAA family members IAA5 and IAA29, which encode the negative regulators of auxin signaling, were locally induced in vascular stem cells and their daughters in Arabidopsis roots. This is an active response to DNA damage in which the transcription factor SUPPRESSOR OF GAMMA RESPONSE 1 directly induces their expression. In the iaa5 iaa29 double mutant, DNA damage-induced stem cell death was significantly suppressed, while it was fully restored by the expression of a stable form of IAA5 in vascular stem cells. Our genetic data revealed that both the suppression of auxin signaling and reduced auxin content are prerequisite for cell death induction, suggesting the central role in maintaining genome integrity in stem cells.One-sentence summaryThe induction of IAA5 and IAA29 promotes stem cell death in Arabidopsis roots under DNA stress.

Plant root growth is influenced by external factors to adapt to changing environmental conditions. However, the mechanisms by which environmental stresses affect root growth remain elusive. Here we found that DNA double-strand breaks (DSBs) induce the expression of genes for the synthesis of cytokinin hormones and enhance the accumulation of cytokinins in the Arabidopsis root tip. This is a programmed response to DSBs through the DNA damage signaling pathway. Our data showed that activation of cytokinin signalling suppresses the expression of PIN-FORMED genes that encode efflux carriers of another plant hormone, auxin, thereby disturbing downward auxin flow and causing cell cycle retardation in the G2 phase. Elevated cytokinin signalling also promotes an early transition from cell division to endoreplication, resulting in a reduction of the root meristem size. We propose that in response to DNA stress, plants inhibit root growth by orchestrating hormone biosynthesis and signalling.

Auxin-Inducible Degron (AID) technology enables conditional depletion of targeted proteins. However, the applicability of the AID in vertebrate cells has been limited due to cytotoxicity caused by high auxin concentrations. Here, we establish an improved AID system using an engineered orthogonal auxin-TIR1 pair, which exhibits over 1,000 times stronger binding. With ~1,000-fold less auxin concentration, we achieved to generate the AID-based knockout cells in various human and mouse cell lines in a single transfection.