Mutual antagonism of ethylene and jasmonic acid regulates ozone-induced spreading cell death in Arabidopsis.
Ethylene (ET) and jasmonic acid (JA) have opposite effects on ozone (O(3))-induced spreading cell death; ET stimulates, and is required for the spreading cell death, whereas JA protects tissues. We studied the underlying molecular mechanisms with the O(3)-sensitive, JA-insensitive jasmonate resistant 1 (jar1), and the O(3)-tolerant, ET-insensitive ethylene insensitive 2 (ein2) mutants. Blocking ET perception pharmacologically with norbornadiene (NBD) in jar1, or ET signaling genetically in the jar1 ein2 double mutant prevented the spread of cell death. This suggests that EIN2 function is epistatic to JAR1, and that the JAR1-dependent JA pathway halts oxidative cell death by directly inhibiting ET signaling. JAR1-dependent suppression of the ET pathway was apparent also as increased EIN2-dependent gene expression and ET hypersensitivity of jar1. Physiological experiments suggested that the target of JA is upstream of Constitutive Triple Response 1 (CTR1), but downstream of ET biosynthesis. Gene expression analysis of 1-aminocyclopropane-1-carboxylic acid (ACC)-treated and O(3)-exposed ein2 and jar1 revealed reciprocal antagonism: the EIN2-mediated suppression of the JA pathway. The results imply that the O(3)-induced spreading cell death is stimulated by early, rapid accumulation of ET, which can suppress the protecting function of JA thereby allowing cell death to proceed. Extended spreading cell death induces late accumulation of JA, which inhibits the propagation of cell death through inhibition of the ET pathway.
Tuominen
Hannele
H
Department of Biological and Environmental Sciences, Plant Biology, University of Helsinki, PO Box 56, Viikinkaari 9, FI-00014 Helsinki, Finland.
Overmyer
Kirk
K
Keinänen
Markku
M
Kollist
Hannes
H
Kangasjärvi
Jaakko
J
D017360:Arabidopsis / Q000187:drug effects* / Q000235:genetics; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D016923:Cell Death / Q000187:drug effects*; D003517:Cyclopentanes / Q000037:antagonists & inhibitors / Q000378:metabolism*; D005030:Ethylenes / Q000037:antagonists & inhibitors / Q000378:metabolism*; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D009154:Mutation; D009713:Nucleotidyltransferases / Q000235:genetics / Q000378:metabolism*; D054883:Oxylipins; D010126:Ozone / Q000494:pharmacology*; D011956:Receptors, Cell Surface / Q000235:genetics / Q000378:metabolism*; D015398:Signal Transduction / Q000187:drug effects; D010453:Peptide Synthases
D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D005030:Ethylenes; D009713:Nucleotidyltransferases; D054883:Oxylipins; D010126:Ozone; D011956:Receptors, Cell Surface; C119963:EIN2 protein, Arabidopsis; C011006:jasmonic acid; C036216:ethylene; C412831:AT2G46370 protein, Arabidopsis; D010453:Peptide Synthases