Hypersensitivity to DNA damage in plant stem cell niches

Abstract

The growing apices of plants contain stem cells that continually produce tissues, which, in the shoot, include the germline. These stem cell populations remain active throughout the plant's life, which can last for centuries, and are particularly exposed to environmental hazards that cause DNA damage and mutations. It is not known whether plants have mechanisms to safeguard the genome specifically in these crucial cell populations. Here, we show that root and shoot stem cells and their early descendants are selectively killed by mild treatment with radiomimetic drugs, x-rays, or mutations that disrupt DNA repair by nonhomologous end-joining. Stem cell death required transduction of DNA damage signals by the ATAXIA-TELANGIECTASIA MUTATED (ATM) kinase and, specifically in the root, also the ATM/RAD3-RELATED (ATR) kinase. Consistent with the absence of p53 and the core apoptotic machinery in plants, death of the stem cells did not show apoptotic but autolytic features as seen in other cases of plant developmentally programmed cell death. We propose that plants have independently evolved selective death as a stringent mechanism to safeguard genome integrity in their stem cell populations.Arabidopsis ͉ double-strand breaks ͉ meristem ͉ programmed cell death

Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis

“…Two recent reports have shown that Arabidopsis root and shoot stem cells and their descendants undergo cell death upon DNA damage (12,28). In the stem cell niche, programmed cell death may be a viable way to remove DNA-damaged cells, but here we found that DSBs induced early onset of endoreduplication in the transition zone of roots and the sepal epidermis.…”

“…To identify plant-specific mechanisms underlying the genotoxic stress response, we first observed Arabidopsis roots that had been exposed to the radiomimetic reagent zeocin (11,12). When seedlings were transferred to 10-μM zeocin plates, root growth was arrested, and cyclin B1 expression (indicative of progression into G2) was reduced ( Fig.…”

“…These results are consistent with our observation that ATR, together with ATM, is associated with inhibition of entry to M phase and endocycle induction. It is interesting that, in root stem cells, UVB-and gamma-induced programmed cell death is activated by SOG1 and by either ATM or ATR (12,28). Although it remains an open question how DNA damage kills Arabidopsis stem cells, G2 arrest may be provoked before cell death by overlapping mechanisms with those involved in DSB-induced endoreduplication.…”

SUPPRESSOR OF GAMMA RESPONSE1 Links DNA Damage Response to Organ Regeneration

“…The aforementioned processes are regulated by positional signals (Heidstra and Sabatini, 2014). Cell-type-specific programmed cell death (PCD) has been observed in root meristems of the model plant Arabidopsis (Arabidopsis thaliana) after exposure to IR, radiomimetic chemicals, UV (Curtis and Hays, 2007;Furukawa et al, 2010;Fulcher and Sablowski, 2009), and chilling stress (Hong et al, 2017). This programmed response requires SOG1, ATM, and (to a lesser degree) ATR as well as de novo protein synthesis (Furukawa et al, 2010).…”

Protection of Arabidopsis Blunt-Ended Telomeres Is Mediated by a Physical Association with the Ku Heterodimer

“…The growth of At13 lines was comparable to wild-type controls, suggesting their proficiency in DNA repair. Plant growth retardation in response to genotoxic stress is caused by preferential cell death of stem cells in meristematic tissues, and Ku deficiency exacerbates this sensitivity (Fulcher and Sablowski, 2009). Therefore, we quantified cell death in the root apical meristem of At18 plants 24 h after treatment with high doses of bleomycin ( Figures 3C and 3D).…”