Spermidine Exodus and Oxidation in the Apoplast Induced by Abiotic Stress Is Responsible for H₂O₂ Signatures That Direct Tolerance Responses in Tobacco

Polyamines (PAs) exert a protective effect against stress challenges, but their molecular role in this remains speculative. In order to detect the signaling role of apoplastic PA-derived hydrogen peroxide (H₂O₂) under abiotic stress, we developed a series of tobacco (Nicotiana tabacum cv Xanthi) tra...

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Published in:	The Plant cell 2008-06, Vol.20 (6), p.1708-1724
Main Authors:	Moschou, Panagiotis N, Paschalidis, Konstantinos A, Delis, Ioannis D, Andriopoulou, Athina H, Lagiotis, George D, Yakoumakis, Dimitrios I, Roubelakis-Angelakis, Kalliopi A
Format:	Article
Language:	eng
Subjects:	Adaptation, Physiological - drug effects Adaptation, Physiological - genetics Adaptation, Physiological - physiology Adenosylmethionine Decarboxylase - genetics Adenosylmethionine Decarboxylase - metabolism Apoptosis - drug effects Biosynthesis Complementary DNA Dose-Response Relationship, Drug Gels Gene Expression Regulation, Plant - drug effects Genes Germination - drug effects Germination - genetics Germination - physiology Hydrogen Peroxide - metabolism Messenger RNA Microscopy, Electron, Transmission Nicotiana - genetics Nicotiana - metabolism Nicotiana - ultrastructure Oxidation-Reduction - drug effects Oxidoreductases Acting on CH-NH Group Donors - genetics Oxidoreductases Acting on CH-NH Group Donors - metabolism Plant cells Plants Plants, Genetically Modified - genetics Plants, Genetically Modified - metabolism Plants, Genetically Modified - ultrastructure Polyamine Oxidase Polyamines Reactive Oxygen Species - metabolism Reverse Transcriptase Polymerase Chain Reaction Salinity Seeds - genetics Seeds - metabolism Seeds - ultrastructure Sodium Chloride - pharmacology Spermidine - metabolism Spermidine - pharmacology Transgenic plants
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Summary:	Polyamines (PAs) exert a protective effect against stress challenges, but their molecular role in this remains speculative. In order to detect the signaling role of apoplastic PA-derived hydrogen peroxide (H₂O₂) under abiotic stress, we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-L-methionine decarboxylase (samdc plants). Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H₂O₂. A-pao plants accumulated less H₂O₂ and exhibited less programmed cell death (PCD) than did wild-type plants, in contrast with S-pao and samdc downregulating plants. Induction of either stress-responsive genes or PCD was dependent on the level of Spd-derived apoplastic H₂O₂. Thus, in wild-type and A-pao plants, stress-responsive genes were efficiently induced, although in the latter at a lower rate, while S-pao plants, with higher H₂O₂ levels, failed to accumulate stress-responsive mRNAs, inducing PCD instead. Furthermore, decreasing intracellular PAs, while keeping normal apoplastic Spd oxidation, as in samdc downregulating transgenic plants, caused enhanced salinity-induced PCD. These results reveal that salinity induces the exodus of Spd into the apoplast, where it is catabolized by PAO, producing H₂O₂. The accumulated H₂O₂ results in the induction of either tolerance responses or PCD, depending also on the levels of intracellular PAs.
ISSN:	1040-4651 1532-298X 1532-298X