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PMID: 22904148 Published · ppublish English Journal Article

Emerging roots alter epidermal cell fate through mechanical and reactive oxygen species signaling.

The Plant cell ·Vol. 24 ·No. 8 ·2012-08-00 ·Pages 3296-306

Steffens B, Kovalev A, Gorb SN, Sauter M

Abstract

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.

MeSH Terms
Amitrole/pharmacology Biomechanical Phenomena Cell Death Cyclopropanes/pharmacology Dose-Response Relationship, Drug Enzyme Inhibitors/pharmacology Ethylenes/pharmacology NADPH Oxidases/antagonists & inhibitors Onium Compounds/pharmacology Organophosphorus Compounds/pharmacology Oryza/drug effects,metabolism,physiology Plant Cells/metabolism,physiology Plant Epidermis/cytology,drug effects,metabolism,physiology Plant Proteins/antagonists & inhibitors,metabolism Plant Roots/drug effects,metabolism,physiology Plant Stems/drug effects,metabolism,physiology Reactive Oxygen Species/metabolism Signal Transduction Stress, Mechanical
Chemicals
Cyclopropanes Enzyme Inhibitors Ethylenes Onium Compounds Organophosphorus Compounds Plant Proteins Reactive Oxygen Species diphenyleneiodonium ethylene NADPH Oxidases 1-methylcyclopropene ethephon Amitrole
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Steffens Bianka
Plant Developmental Biology and Plant Physiology, Institute of Botany, University of Kiel, 24118 Kiel, Germany.
Kovalev Alexander
Gorb Stanislav N
Sauter Margret
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Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
DOI
10.1105/tpc.112.101790
Published
2012-08-00
Epub
2012-00-17
Pages
3296-306
Language
English
Region
England
NLM ID
9208688
PMCID
PMC3462632
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.112.101790 PMC Full Text View journal details
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