A Sacrifice-for-Survival Mechanism Protects Root Stem Cell Niche from Chilling Stress

Temperature has a profound influence on plant and animal development, but its effects on stem cell behavior and activity remain poorly understood. Here, we characterize the responses of the Arabidopsis root to chilling (low but above-freezing) temperature. Chilling stress at 4°C leads to DNA damage...

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Bibliographic Details
Published in:Cell 2017-06, Vol.170 (1), p.102-113.e14
Main Authors: Hong, Jing Han, Savina, Maria, Du, Jing, Devendran, Ajay, Kannivadi Ramakanth, Karthikbabu, Tian, Xin, Sim, Wei Shi, Mironova, Victoria V., Xu, Jian
Format: Article
Language:English
Subjects:
Arabidopsis - physiology
auxin maximum
Cell Division
chilling stress
Cold Temperature
DNA damage
Indoleacetic Acids - metabolism
Plant Roots - cytology
Plant Roots - physiology
selective cell death
Stem Cell Niche
stem cell survival
Stem Cells - cytology
Stress, Physiological
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Summary:Temperature has a profound influence on plant and animal development, but its effects on stem cell behavior and activity remain poorly understood. Here, we characterize the responses of the Arabidopsis root to chilling (low but above-freezing) temperature. Chilling stress at 4°C leads to DNA damage predominantly in root stem cells and their early descendants. However, only newly generated/differentiating columella stem cell daughters (CSCDs) preferentially die in a programmed manner. Inhibition of the DNA damage response in these CSCDs prevents their death but makes the stem cell niche more vulnerable to chilling stress. Mathematical modeling and experimental validation indicate that CSCD death results in the re-establishment of the auxin maximum in the quiescent center (QC) and the maintenance of functional stem cell niche activity under chilling stress. This mechanism improves the root’s ability to withstand the accompanying environmental stresses and to resume growth when optimal temperatures are restored. [Display omitted] •Chilling stress causes DNA damage in root stem cells and their early descendants•Chilling stress induces protective death of columella stem cell daughters (CSCDs)•CSCD death re-establishes QC auxin maximum and prevents further division of CSCs•CSCD death improves the root’s ability to withstand other stresses and to recover Arabidopsis roots protect their stem cell niche from chilling stress via a selective cell death mechanism regulated by auxin and DNA damage response.
ISSN:0092-8674
1097-4172
DOI:10.1016/j.cell.2017.06.002