Emerging roots alter epidermal cell fate through mechanical and reactive oxygen species signaling.
A central question in biology is how spatial information is conveyed to locally establish a developmental program. Rice (Oryza sativa) can survive flash floods by the emergence of adventitious roots from the stem. Epidermal cells that overlie adventitious root primordia undergo cell death to facilitate root emergence. Root growth and epidermal cell death are both controlled by ethylene. This study aimed to identify the signal responsible for the spatial control of cell death. Epidermal cell death correlated with the proximity to root primordia in wild-type and ADVENTITIOUS ROOTLESS1 plants, indicating that the root emits a spatial signal. Ethylene-induced root growth generated a mechanical force of ~18 millinewtons within 1 h. Force application to epidermal cells above root primordia caused cell death in a dose-dependent manner and was inhibited by 1-methylcyclopropene or diphenylene iodonium, an inhibitor of NADPH oxidase. Exposure of epidermal cells not overlying a root to either force and ethylene or force and the catalase inhibitor aminotriazole induced ectopic cell death. Genetic downregulation of the reactive oxygen species (ROS) scavenger METALLOTHIONEIN2b likewise promoted force-induced ectopic cell death. Hence, reprogramming of epidermal cell fate by the volatile plant hormone ethylene requires two signals: mechanosensing for spatial resolution and ROS for cell death signaling.
Plant Developmental Biology and Plant Physiology, Institute of Botany, University of Kiel, 24118 Kiel, Germany.
Bianka
B
Steffens
Alexander
A
Kovalev
Stanislav N
SN
Gorb
Margret
M
Sauter
D000640:Amitrole / Q000494:pharmacology; D001696:Biomechanical Phenomena; D016923:Cell Death; D003521:Cyclopropanes / Q000494:pharmacology; D004305:Dose-Response Relationship, Drug; D004791:Enzyme Inhibitors / Q000494:pharmacology; D005030:Ethylenes / Q000494:pharmacology; D019255:NADPH Oxidases / Q000037:antagonists & inhibitors; D009861:Onium Compounds / Q000494:pharmacology; D009943:Organophosphorus Compounds / Q000494:pharmacology; D012275:Oryza / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D059828:Plant Cells / Q000378:metabolism / Q000502:physiology; D019441:Plant Epidermis / Q000166:cytology / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D010940:Plant Proteins / Q000037:antagonists & inhibitors / Q000378:metabolism; D018517:Plant Roots / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D018547:Plant Stems / Q000187:drug effects / Q000378:metabolism / Q000502:physiology; D017382:Reactive Oxygen Species / Q000378:metabolism*; D015398:Signal Transduction; D013314:Stress, Mechanical
D003521:Cyclopropanes; D004791:Enzyme Inhibitors; D005030:Ethylenes; D009861:Onium Compounds; D009943:Organophosphorus Compounds; D010940:Plant Proteins; D017382:Reactive Oxygen Species; C007517:diphenyleneiodonium; C036216:ethylene; D019255:NADPH Oxidases; C412563:1-methylcyclopropene; C005073:ethephon; D000640:Amitrole