The transcriptional repressors IAA5 and IAA29 participate in DNA damage-induced stem cell death in Arabidopsis roots.

Abstract

Plants generate organs continuously during post-embryonic development. Thus, their ability to preserve stem cells in changing environments is crucial for their survival. Genotoxic stress threatens genome stability in all somatic cells. However, in the meristem, only the stem cells actively die in response to DNA damage, followed by stem cell replenishment that guarantees genome stability in these cells. Cytokinin biosynthesis-induced inhibition of downward auxin flow participates in DNA damage-induced stem cell death in roots. Without this system, stem cell death occurs at a reduced but significant level, suggesting another mechanism governing the DNA damage response in stem cells. Here, we demonstrate that in response to DNA double-strand breaks, the AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) family members IAA5 and IAA29, encoding negative regulators of auxin signaling, are induced in Arabidopsis (Arabidopsis thaliana) roots. The transcription factor SUPPRESSOR OF GAMMA RESPONSE 1 directly induces their expression as an active response to DNA damage. In the iaa5 iaa29 double mutant, DNA damage-induced stem cell death is greatly suppressed, while it is fully restored by the expression of a stable form of IAA5 in vascular stem cells. Our genetic data reveal that reduced auxin signaling around the stem cell niche, caused by IAA5 and IAA29 induction and enhanced cytokinin biosynthesis, is a prerequisite for cell death induction, thus playing a central role in maintaining genome integrity in root stem cells.